Out of Shape During Stress: A Key Role for Auxin

Abstract

In most abiotic stress conditions, including salinity and water deficit, the developmental plasticity of the plant root is regulated by the phytohormone auxin. Changes in auxin concentration are often attributed to changes in shoot-derived long-distance auxin flow. However, recent evidence suggests important contributions by short-distance auxin transport from local storage and local auxin biosynthesis, conjugation, and oxidation during abiotic stress. We discuss here current knowledge on long-distance auxin transport in stress responses, and subsequently debate how short-distance auxin transport and indole-3-acetic acid (IAA) metabolism play a role in influencing eventual auxin accumulation and signaling patterns. Our analysis stresses the importance of considering all these components together and highlights the use of mathematical modeling for predictions of plant physiological responses.

Keywords: IAA homeostasis; abiotic stress; auxin; auxin transport; mathematical modeling; root phenotypic plasticity.

Figure 1

Schematic Overview of Salt Stress-Induced Changes in Auxin Biosynthesis, Conjugation, and Transport-Related Processes in the Arabidopsis Roots. (A) Indole-3-acetic acid (IAA) metabolism. The level of IAA is tightly regulated by IAA biosynthesis, conjugation, and degradation, together determining the IAA status of a cell. The lower panel shows part of the known IAA biosynthesis (, for a complete overview) and conjugation pathways and the known involved genes or gene families. Based on microarray data of two different studies (Table S1), we have identified gene expression patterns with promising possibilities for influencing eventual IAA accumulation patterns and signaling. For genes in the IAOx pathway we observe strong expression in zone 4 (Figure 2C), which is the zone containing primordia and lateral roots. All genes are also influenced by salt stress in a time-dependent matter (Table S1). We see a similar pattern for DAO1 and DAO2. Both DAO1 and CYP79B2-3 have been linked to lateral root development and show expression specifically underlying newly formed lateral roots. YUCCA 3, 5, 8, and 9, together with the GH3 family genes, show upregulation in the epidermis and cortex during salt stress, whereas they are downregulated in the columnella (Figure 2B). (B) Auxin transport. During salt stress, expression of the auxin efflux carriers PIN1, PIN7, and ABCB19 in the stele is downregulated. In the columnella, PIN3 and PIN7 are downregulated. In epidermal and cortical cells, PIN2 and ABCB4 auxin efflux carriers are downregulated whereas ABCB1 is slightly upregulated. In epidermal cells, on a cellular level, PIN2 is internalized and changes in AUX1 abundance at the plasma membrane during halotropism were observed, providing evidence that AUX1 is also internalized . Putatively, the activity of the tonoplast-located WAT1 undergoes changes to alter intracellular auxin levels following a change in cytosolic pH. To create local auxin maxima, the passive flow of IAA⁻ molecules through the plasmodesmata (PD) might need to be blocked. This is putatively achieved through GSL8-mediated callose deposition. The apoplastic pH increase following salt exposure of the root potentially inhibits the passive influx of IAAH into the cell. Blue arrows depict auxin flow, grey boxes show up- (green arrow) or downregulation (red arrow) of genes during salt stress. Black boxes show plasma-membrane proteins that are internalized upon salt stress. Question marks show processes that influence local auxin concentrations but have not yet been proved to be involved in local auxin changes during abiotic stress. Abbreviations: IAA⁻, ionized IAA; IAA-glc, IAA-glucose; IAAH, protonated IAA; IAN, indole-3-acetonitrile; IAOx, indole-3-acetaldoxime; IPyA, indole-3-pyruvic acid; oxIAA, oxidized IAA (2-oxindole-3-acetic acid); PD, plasmodesma; Trp, tryptophan.

Figure 2

Illustration of Gene Expression of Auxin Homeostasis-Related Genes Showing Patterns That Could Be Relevant for Indole-3-Acetic acid (IAA) Accumulation Patterns in Abiotic Stress. (A) Heatmaps are based on microarray data of two different studies (Table S1) , . For tissue-specific and zone specific expression patterns, the root has been divided in different tissues and in four different root zones, as illustrated. Figure adapted, with permission, from Figshare (B. Peret, Primary and lateral root.ai; https://figshare.com/collections/Root_illustrations/3701038). (B) Heatmap of the relative expression (log₂ fold change) upon salt stress of YUC3, 5, 8, and 9 in different root tissues. (C) Heatmap of the expression of genes in the indole-3-acetaldoxime (IAOx) pathway and oxidation in different root zones under control conditions and during salt stress. The heatmap is normalized per gene. (D) Heatmap of the expression of genes involved in IAA conjugation in the shoot and root under control conditions and during salt stress. The heatmap is normalized per gene.